Butterfly wing color scales an evolutionary canvas

The evolution of insect wings provided a new patterning surface that has been exploited in many ways by a variety of insect lineages. One of the most striking is the evolution of rows of pigmented scales that cover the wings of butterflies and moths (Lepidoptera). The shinglelike pigmented structural scales form the individual units of butterfly wing color patterns. Scales can exhibit a wide range of colors, shapes, and microarchitectures, both within and between butterfly species. Butterfly scales are also used for thermoregulation and predator avoidance. The array of thousands of overlapping scales on a butterfly wing surface represents a canvas on which a dazzling variety of colors and patterns has evolved.

Butterfly scales represent another morphological novelty that is derived from a preexisting structure—in this case, the innervated bristles that are common to all insects. The early cell lineage of butterfly wing scale development resembles the cell lineage that forms insect bristles (Fig. 6.3a). Each insect bristle consists of four distinct cell types: a bristle cell, a socket cell, a neuron, and a glial (sheath) cell. All four types originate from a single precursor, the sensory mother cell (SMC). The SMC divides to create the pIIa and pIIb cells; pIIa cells then divide again to create a bristle and a socket cell, and pIIb cells divide to create a neuron and a glial cell. By contrast, butterfly structural scales are made up of two cells, a scale cell and a socket cell, and are not innervated. The precursor cell for butterfly scales divides. While one daughter then divides again to create the socket and scale cells (similar to pIIa), the other daughter cell dies.

Figure 6.3

Butterfly scales evolved from insect bristles

(a) The cell lineage characteristic of insect sensory bristles is similar to the formation of butterfly scales. The butterfly ASH1 gene, a homolog of the achaete-scute bHLH gene family, is expressed in both bristles (not shown) and in developing scale precursor cells

Butterfly scales evolved from insect bristles

(a) The cell lineage characteristic of insect sensory bristles is similar to the formation of butterfly scales. The butterfly ASH1 gene, a homolog of the achaete-scute bHLH gene family, is expressed in both bristles (not shown) and in developing scale precursor cells

The evolutionary relationship between butterfly scales and insect bristles is reflected by regulatory gene expression within these cell lineages. The transcription factors that are expressed early in insect bristle development and that are required for bristle formation comprise the bHLH genes of the Achaete-Scute Complex (AS-C). A butterfly homolog of these genes (ASH1) is expressed both during butterfly sensory bristle formation and in the segregating scale precursor cells that are aligned in rows across the developing wing (Fig. 6.3b). The expression of ASH1 during butterfly scale formation supports the hypothesis that early scale development is homologous to insect bristle formation.

At least three novel aspects of developmental gene regulation have generated the unique spatial distribution, cytoarchitecture, and pigmentation of butterfly wing scales. One involves the expanded expression of an AS-C gene in rows of cells across the entire surface of the developing butterfly wing. A second regulatory change is the evolution of a set of target genes deployed within scale cells that generates the flattened, rigid cytoarchitecture of butterfly wing scales. A third aspect of regulatory evolution is the recruitment of genes in the pigmentation pathway to be expressed in scale cells, thereby creating an array of colored

Figure 6.4

Butterfly eyespot foci are marked by Dll expression

The adult hindwings of Precis coenia (a) and Bicyclus anynana (b) illustrate some of the variety seen in terms of number and coloration of eyespots between butterfly species. (c,d) Dll protein is expressed in larval stages along the wing edge in circular groups of cells of the presumptive eyespot foci. Two foci appear in Precis hindwings (c, arrows) and seven in Bicyclus hindwings (d). Source: Brakefield PM, Gates J, Keys D, et al. Development, plasticity and evolution of butterfly eyespot patterns. Nature 1996; 384: 236-242.

Figure 6.4

Butterfly eyespot foci are marked by Dll expression

The adult hindwings of Precis coenia (a) and Bicyclus anynana (b) illustrate some of the variety seen in terms of number and coloration of eyespots between butterfly species. (c,d) Dll protein is expressed in larval stages along the wing edge in circular groups of cells of the presumptive eyespot foci. Two foci appear in Precis hindwings (c, arrows) and seven in Bicyclus hindwings (d). Source: Brakefield PM, Gates J, Keys D, et al. Development, plasticity and evolution of butterfly eyespot patterns. Nature 1996; 384: 236-242.

scales on the adult wing. Collectively, these innovations created a canvas upon which additional regulatory systems control the spatial patterning of colored wing scales.